Contrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses

Abstract NACs are plant-specific transcription factors involved in controlling plant development, stress responses, and senescence. As senescence-associated genes (SAGs), NACs integrate age- and stress-dependent pathways that converge to programmed cell death (PCD). In Arabidopsis, NAC-SAGs belong t...

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Autores principales: Bruno Paes Melo, Isabela Tristan Lourenço-Tessutti, Otto Teixeira Fraga, Luanna Bezerra Pinheiro, Camila Barrozo de Jesus Lins, Carolina Vianna Morgante, Janice Almeida Engler, Pedro Augusto Braga Reis, Maria Fátima Grossi-de-Sá, Elizabeth Pacheco Batista Fontes
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spelling oai:doaj.org-article:eeaf472185ca4f26aca654521a107d932021-12-02T14:49:10ZContrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses10.1038/s41598-021-90767-62045-2322https://doaj.org/article/eeaf472185ca4f26aca654521a107d932021-05-01T00:00:00Zhttps://doi.org/10.1038/s41598-021-90767-6https://doaj.org/toc/2045-2322Abstract NACs are plant-specific transcription factors involved in controlling plant development, stress responses, and senescence. As senescence-associated genes (SAGs), NACs integrate age- and stress-dependent pathways that converge to programmed cell death (PCD). In Arabidopsis, NAC-SAGs belong to well-characterized regulatory networks, poorly understood in soybean. Here, we interrogated the soybean genome and provided a comprehensive analysis of senescence-associated Glycine max (Gm) NACs. To functionally examine GmNAC-SAGs, we selected GmNAC065, a putative ortholog of Arabidopsis ANAC083/VNI2 SAG, and the cell death-promoting GmNAC085, an ANAC072 SAG putative ortholog, for analyses. Expression analysis of GmNAC065 and GmNAC085 in soybean demonstrated (i) these cell death-promoting GmNACs display contrasting expression changes during age- and stress-induced senescence; (ii) they are co-expressed with functionally different gene sets involved in stress and PCD, and (iii) are differentially induced by PCD inducers. Furthermore, we demonstrated GmNAC065 expression delays senescence in Arabidopsis, a phenotype associated with enhanced oxidative performance under multiple stresses, higher chlorophyll, carotenoid and sugar contents, and lower stress-induced PCD compared to wild-type. In contrast, GmNAC085 accelerated stress-induced senescence, causing enhanced chlorophyll loss, ROS accumulation and cell death, decreased antioxidative system expression and activity. Accordingly, GmNAC065 and GmNAC085 targeted functionally contrasting sets of downstream AtSAGs, further indicating that GmNAC85 and GmNAC065 regulators function inversely in developmental and environmental PCD.Bruno Paes MeloIsabela Tristan Lourenço-TessuttiOtto Teixeira FragaLuanna Bezerra PinheiroCamila Barrozo de Jesus LinsCarolina Vianna MorganteJanice Almeida EnglerPedro Augusto Braga ReisMaria Fátima Grossi-de-SáElizabeth Pacheco Batista FontesNature PortfolioarticleMedicineRScienceQENScientific Reports, Vol 11, Iss 1, Pp 1-21 (2021)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Bruno Paes Melo
Isabela Tristan Lourenço-Tessutti
Otto Teixeira Fraga
Luanna Bezerra Pinheiro
Camila Barrozo de Jesus Lins
Carolina Vianna Morgante
Janice Almeida Engler
Pedro Augusto Braga Reis
Maria Fátima Grossi-de-Sá
Elizabeth Pacheco Batista Fontes
Contrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses
description Abstract NACs are plant-specific transcription factors involved in controlling plant development, stress responses, and senescence. As senescence-associated genes (SAGs), NACs integrate age- and stress-dependent pathways that converge to programmed cell death (PCD). In Arabidopsis, NAC-SAGs belong to well-characterized regulatory networks, poorly understood in soybean. Here, we interrogated the soybean genome and provided a comprehensive analysis of senescence-associated Glycine max (Gm) NACs. To functionally examine GmNAC-SAGs, we selected GmNAC065, a putative ortholog of Arabidopsis ANAC083/VNI2 SAG, and the cell death-promoting GmNAC085, an ANAC072 SAG putative ortholog, for analyses. Expression analysis of GmNAC065 and GmNAC085 in soybean demonstrated (i) these cell death-promoting GmNACs display contrasting expression changes during age- and stress-induced senescence; (ii) they are co-expressed with functionally different gene sets involved in stress and PCD, and (iii) are differentially induced by PCD inducers. Furthermore, we demonstrated GmNAC065 expression delays senescence in Arabidopsis, a phenotype associated with enhanced oxidative performance under multiple stresses, higher chlorophyll, carotenoid and sugar contents, and lower stress-induced PCD compared to wild-type. In contrast, GmNAC085 accelerated stress-induced senescence, causing enhanced chlorophyll loss, ROS accumulation and cell death, decreased antioxidative system expression and activity. Accordingly, GmNAC065 and GmNAC085 targeted functionally contrasting sets of downstream AtSAGs, further indicating that GmNAC85 and GmNAC065 regulators function inversely in developmental and environmental PCD.
format article
author Bruno Paes Melo
Isabela Tristan Lourenço-Tessutti
Otto Teixeira Fraga
Luanna Bezerra Pinheiro
Camila Barrozo de Jesus Lins
Carolina Vianna Morgante
Janice Almeida Engler
Pedro Augusto Braga Reis
Maria Fátima Grossi-de-Sá
Elizabeth Pacheco Batista Fontes
author_facet Bruno Paes Melo
Isabela Tristan Lourenço-Tessutti
Otto Teixeira Fraga
Luanna Bezerra Pinheiro
Camila Barrozo de Jesus Lins
Carolina Vianna Morgante
Janice Almeida Engler
Pedro Augusto Braga Reis
Maria Fátima Grossi-de-Sá
Elizabeth Pacheco Batista Fontes
author_sort Bruno Paes Melo
title Contrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses
title_short Contrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses
title_full Contrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses
title_fullStr Contrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses
title_full_unstemmed Contrasting roles of GmNAC065 and GmNAC085 in natural senescence, plant development, multiple stresses and cell death responses
title_sort contrasting roles of gmnac065 and gmnac085 in natural senescence, plant development, multiple stresses and cell death responses
publisher Nature Portfolio
publishDate 2021
url https://doaj.org/article/eeaf472185ca4f26aca654521a107d93
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